The Potential Roles of Eutrophication and Climate Change

Harmful Algae 14 (2012) 313–334

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Harmful Algae

jo urnal homepage: www.elsevier.com/locate/hal

The rise of harmful cyanobacteria blooms: The potential roles of eutrophication and climate change

a, b b c

J.M. O’Neil *, T.W. Davis , M.A. Burford , C.J. Gobler

University of Maryland, Center for Environmental Science, Horn Point Laboratory, Cambridge, MD 21613, USA

Grifﬁth University, Australian Rivers Institute, Nathan, QLD 4111, Australia

Stony Brook University, School of Marine and Atmospheric Science, Stony Brook, NY, USA

A R T I C L E I N F O A B S T R A C T

Article history: Cyanobacteria are the most ancient phytoplankton on the planet and form harmful algal blooms in

Available online 29 October 2011

freshwater, estuarine, and marine ecosystems. Recent research suggests that eutrophication and climate

change are two processes that may promote the proliferation and expansion of cyanobacterial harmful

Keywords: algal blooms. In this review, we speciﬁcally examine the relationships between eutrophication, climate

Climate change

change and representative cyanobacterial genera from freshwater (Microcystis, Anabaena, Cylindros-

Cyanobacteria

permopsis), estuarine (Nodularia, Aphanizomenon), and marine ecosystems (Lyngbya, Synechococcus,

CyanoHABs

Trichodesmium). Commonalities among cyanobacterial genera include being highly competitive for low

Eutrophication

concentrations of inorganic P (DIP) and the ability to acquire organic P compounds. Both diazotrophic (=

Harmful algae blooms

Toxins nitrogen (N2) ﬁxers) and non-diazotrophic cyanobacteria display great ﬂexibility in the N sources they

exploit to form blooms. Hence, while some cyanobacterial blooms are associated with eutrophication,

several form blooms when concentrations of inorganic N and P are low. Cyanobacteria dominate

phytoplankton assemblages under higher temperatures due to both physiological (e.g. more rapid

growth) and physical factors (e.g. enhanced stratiﬁcation), with individual species showing different

temperature optima. Signiﬁcantly less is known regarding how increasing carbon dioxide (CO2)

concentrations will affect cyanobacteria, although some evidence suggests several genera of

cyanobacteria are well-suited to bloom under low concentrations of CO2. While the interactive effects

of future eutrophication and climate change on harmful cyanobacterial blooms are complex, much of the

current knowledge suggests these processes are likely to enhance the magnitude and frequency of these

events.

1. Introduction harmful cyanobacterial blooms have included increased nutrient

inputs, the transport of cells or cysts via anthropogenic activities,

While cyanobacterial harmful algal blooms have been reported and increased aquaculture production and/or overﬁshing that

in the scientiﬁc literature for more than 130 years (Francis, 1878), alters food webs and may permit harmful species to dominate algal

in recent decades, the incidence and intensity of these blooms, as communities (GEOHAB, 2001; HARRNESS, 2005; Heisler et al.,

well as economic loss associated with these events has increased in 2008). It has also been shown that an increase in surface water

both fresh and marine waters (Chorus and Bartram, 1999; temperatures due to changing global climate could play a role in

Carmichael, 2001, 2008; Hudnell, 2008; Heisler et al., 2008; the proliferation of cyanobacterial blooms (Peperzak, 2003; Paerl

Hoagland et al., 2002; Paerl, 2008; Paul, 2008; Paerl and Huisman, and Huisman, 2008; Paul, 2008). Importantly, there is consensus

2008). Recently, there have been discoveries of previously that harmful algal blooms are complex events, typically not caused

unidentiﬁed cyanobacterial toxins, such as amino b-methyla- by a single environmental driver but rather multiple factors

mino-L-alanine (BMAA), and of new genera of cyanobacteria occurring simultaneously (Heisler et al., 2008). Finally, an

capable of producing previously described toxins (Cox et al., 2003, improved ability to detect and monitor harmful cyanobacterial

2005, 2009; Cox, 2009; Brand, 2009; Kerbrat et al., 2011). To date, blooms, and their toxins as well as increased scientiﬁc and public

factors identiﬁed as contributing towards the global expansion of awareness of these events has also led to better documentation of

these events (GEOHAB, 2001; HARRNESS, 2005; Sivonen and

Bo¨rner, 2008).

There have been several reviews of the intensiﬁcation and

* Corresponding author.

E-mail address: [email protected] (J.M. O’Neil). global expansion of harmful cyanobacterial blooms in terms of

314 J.M. O’Neil et al. / Harmful Algae 14 (2012) 313–334

both abundance, geographic extent, and effects on ecosystem in the Baltic Sea, an ecosystem whose primary production is

health, as well as factors that may be facilitating this expansion dominated by cyanobacteria, BMAA has been measured in

(Paerl, 1988, 1997; Paerl and Millie, 1996; Soranno, 1997; significant quantities in both fish and shellfish (Jonasson et al.,

Carmichael, 2001; Saker and Grifﬁths, 2001; Landsberg, 2002; 2010).

Codd et al., 2005a,b; Huisman and Hulot, 2005; see multiple papers

in Hudnell, 2008). The purpose of this review is to: (1) Highlight 2.2. Nutrients

important ﬁndings of the last decade of harmful cyanobacterial

bloom research in fresh, estuarine and marine environments; and Of all of the potential environmental drivers behind harmful

(2) Describe how factors associated with eutrophication and algal and cyanobacterial blooms, the one that has received the

climate change affect some of the most widely studied harmful most attention among the global scientiﬁc community has been

cyanobacterial bloom genera. anthropogenic nutrient pollution. Research indicates that cultural

eutrophication associated with the increased global human

2. Background population has stimulated the occurrences of harmful algal blooms

(Anderson, 1989; Hallegraeff, 1993; Burkholder, 1998; Anderson

Cyanobacteria are prokaryotes but have historically been et al., 2002; Glibert et al., 2005; Glibert and Burkholder, 2006;

grouped with eukaryotic ‘‘algae’’ and at varying times have been Heisler et al., 2008). As bodies of freshwater become enriched in

referred to as: blue–greens, blue–green algae, Myxophyceae, nutrients, especially phosphorus (P), there is often a shift in the

Cyanophyceae and Cyanophyta (Carmichael, 2008). More recently phytoplankton community towards dominance by cyanobacteria

cyanobacteria that form harmful blooms have been termed (Smith, 1986; Trimbee and Prepas, 1987; Watson et al., 1997; Paerl

‘‘CyanoHABs’’ (Carmichael, 2001, 2008; Paerl, 2008) or ‘‘cyano- and Huisman, 2009). Examples of these changes are the dense

bacterial blooms’’ (Hudnell et al., 2008). blooms often found in newly eutrophied lakes, reservoirs, and

rivers previously devoid of these events (Fogg, 1969; Reynolds and

2.1. Toxins Walsby, 1975; Reynolds, 1987; Paerl, 1988, 1997). Empirical

models predict that in temperate ecosystems, summer phyto-

Many genera of cyanobacteria are known to produce a wide plankton communities will be potentially dominated by cyano-

variety of toxins and bioactive compounds, which are secondary bacteria at total phosphorus (TP) concentrations of 100–

À1

metabolites (i.e. compounds not essential to the cyanobacteria for 1000 mg L (Trimbee and Prepas, 1987; Jensen et al., 1994;

growth or its own metabolism) (Sivonen and Jones, 1999). Toxins Watson et al., 1997; Downing et al., 2001).

generally refer to compounds that cause animal and human One reason that P often controls the proliferation of freshwater

poisonings or health risks, and bioactive compounds refer to ecosystems is that many cyanobacteria that bloom in warm waters

compounds that can have antimicrobial and cytotoxic properties have the ability to ﬁx nitrogen (N; Paerl, 1988; Paerl et al., 2001).

and are often of interest in pharmaceutical and as research tools Since many of the bloom forming cyanobacteria genera are not

(Codd et al., 2005a,b). While many of these compounds have diazotrophic and the proliferation of some blooms may be limited

recognized toxic effects, the impact and long term effects of many by N (Gobler et al., 2007; Davis et al., 2010), it has been

of these compounds is unknown (Tonk, 2007). hypothesized both N and P may control harmful cyanobacterial

Hepatotoxins are globally the most prevalent cyanobacterial blooms (Paerl et al., 2008; Paerl and Huisman, 2009). While

toxins followed by neurotoxins (Sivonen and Jones, 1999; Klisch research on cyanobacterial blooms has traditionally considered

and Ha¨der, 2008; Sivonen and Bo¨rner, 2008). Hepatotoxins inorganic N and P pools as being accessed by cyanobacteria or total

include: (1) microcystins, (2) nodularins, and (3) cylindrosper- N and P pools for understanding the trophic state of ecosystems,

mopsins. The three most commonly produced types of cyano- recent research has demonstrated that organic N and P may be

bacterial neurotoxins are: (1) anatoxin-a, (2) anatoxin-a (S), and important nutrient sources for cyanobacteria. Much of the soluble

(3) saxitoxins. As noted above, Cox et al. (2003, 2005) recently N and P pools in most aquatic environments are comprised of

described the presence of the neurotoxic compound, BMAA in organic compounds (Franko and Heath, 1979; Seitzinger and

nearly all cyanobacteria they tested (Table 1). It has been Sanders, 1997; Kolowith et al., 2001) and many cyanobacteria can

hypothesized that BMAA may be a possible cause of the utilize various forms of dissolved and particulate organic N and P

amyotrophic lateral sclerosis parkinsonism–dementia complex (Glibert and Bronk, 1994; Paerl, 1988; Paerl and Millie, 1996;

(ALS-PDC; Cox et al., 2003, 2009; Murch et al., 2004; Cox, 2009). As Pinckney et al., 1997; Berman and Chava, 1999; Glibert and O’Neil,

such, the discovery that this compound is potentially produced by 1999; Davis et al., 2010). Since neither inorganic nutrient pools nor

a broad range of cyanobacteria greatly increases the potential for nutrients ratios typically are able to sufﬁciently explain the

human exposure (Sivonen and Bo¨rner, 2008; Brand, 2009). Indeed, extended duration of dense cyanobacterial blooms (Heisler et al.,

Table 1

Major cyanobacterial bloom toxins.

Toxin group Primary target organ in mammals Cyanobactrial genera

Microcystins Liver Microcystis, Anabaena, Planktothrix (Oscillatoria), Nostoc, Hapalosiphon, Anabaenopsis,

Trichodesmium, Synechococcus, Snowella

Nodularian Liver Nodularia

Cylindrospermopsin Liver Cylindrospermopsis, Umezakia, Aphanizomenon, Lyngbya, Raphidiopsis, Anabaena

Anatoxin-a Nerve synapse Anabaena, Planktothrix (Oscillatoria), Aphanizomenon, Phormidium, Rhaphidiopsis

Anatoxin-a(S) Nerve synapse Anabaena

Saxitoxins Nerve axons Anabaena, Planktothrix (Oscillatoria), Aphanizomenon, Lyngbya, Cylindrospermopsis,

Scytonema

Palytoxins Nerve axons Trichodesmium

Aplysiatoxins Skin Lyngbya, Schizothrix, Planktothrix (Oscillatoria)

Lyngbyatoxin-a Skin, gatro-intestinal tract Lyngbya

Lipopolysaccharides Irritant; affects exposed tissue All

BMAA Nerve synapse All

Sources: Chorus and Bartram (1999), Li et al. (2001a), Codd et al. (2005a,b), Humpage (2008), Klisch and Ha¨der (2008), Smith et al. (2011).

J.M. O’Neil et al. / Harmful Algae 14 (2012) 313–334 315

2008; Paerl, 2008), research of these events must consider the individual cyanobacterial taxa to rising temperatures will be diverse

impacts of all nutrient species, including micro-nutrients. Iron (Fe) and has not been reviewed in detail to date.

has also been found to be an important micro-nutrient in

determining cyanobacterial bloom abundance, especially for 2.3.2. Carbon dioxide and pH

diazotrophs, given that the enzyme nitrogenase has a high Fe The combustion of fossil fuels during the past two centuries has

requirement (Kustka et al., 2003). The recent expansion of signiﬁcantly increased concentrations of atmospheric carbon

molecular investigations of cyanobacteria has permitted a clearer dioxide (CO2), a trend that is projected to continue in the coming

understanding of the manner in which harmful cyanobacterial decades (IPCC, 2007). Atmospheric CO2 concentrations that had

bloom species respond to all nutrients at the cellular level. previously increased at a rate of 1% per year in the 20th century are

Importantly, there are diverse responses to nutrient sources and now increasing 3% per year and may exceed 800 ppm by the end

concentrations among cyanobacterial blooms species that will be of this century (IPCC, 2007; Fu¨ ssel, 2009). Aquatic chemistry will

highlighted in this review. be strongly altered by this rising CO2 as levels of both pH and

carbonate ions will decline (Cao and Caldeira, 2008).

2.3. Climate change The pH of aquatic water bodies is intimately linked to the

speciation of dissolved inorganic carbon (DIC) (e.g. CO2; carbonic

À 3À

The sum of research conducted regarding the evolutionary acid H2CO3; bicarbonate HCO3 ; or carbonate CO2 ) and the pH of

history, ecophysiology, and in situ dynamics of cyanobacteria most systems (7.5–8.1) maintains inorganic carbon primarily in

suggests that they will thrive under the conditions predicted for the form of HCO3 . The buffering capacity of marine ecosystems

global climate change (Paul, 2008; Paerl and Huisman, 2009). The maintains the pH and speciation of inorganic DIC in a smaller range

details of how speciﬁc genera of cyanobacteria may respond to than those typically observed in freshwaters. Many lakes are

climate change, however, are less clear. This review will focus on supersaturated with CO2 (Cole et al., 1994; Maberly, 1996) due to

the speciﬁc effects of temperature and concomitant changes in terrestrial C inputs and sediment respiration (Cole et al., 1994). The

stratiﬁcation, as well as the effect of CO2 and pH on multiple pH and speciation of inorganic carbon in lakes can vary widely on a

freshwater, estuarine, and marine cyanobacteria genera. scale from daily (diel), to episodic, to seasonal (Maberly, 1996; Qui

and Gao, 2002) with diel variations in productive lakes as high as 2

À1

2.3.1. Temperature pH units and 60 mmol DIC L (Maberly, 1996). The large, diel

The burning of fossil fuels and subsequent rise in atmospheric drawdown in DIC associated with algal blooms in eutrophic lakes

carbon dioxide has caused the earth’s surface temperature to may cause phytoplankton to become ephemerally C-limited. It has

increase by approximately 1 8C during the 20th century, with most been hypothesized that surface-dwelling cyanobacteria may have

of the increase having occurred during the last 40 years (IPCC, an advantage over other phytoplankton due to their closer

2007). In the current century, global temperatures are expected to proximity to atmospheric CO2 that may rapidly diffuse into

increase an additional 1.5–5 8C (Houghton et al., 2001; IPCC, 2007). surface waters and promote their growth when water column CO2

Natural communities of phytoplankton have been and will concentrations are drawn down by dense blooms (Paerl and

continue to be inﬂuenced by these increases in temperature as Huisman, 2009). Alternatively, there is evidence that low DIC

algal growth rates are strongly, but differentially, temperature environments may favor cyanobacteria. Several studies have

dependent (Eppley, 1972; Goldman and Carpenter, 1974; Raven reported that cyanobacteria out-compete eukaryotic algae under

and Geider, 1988). As temperatures approach and exceed 20 8C, the high pH and low CO2 conditions (Shapiro and Wright, 1990; Oliver

growth rates of freshwater eukaryotic phytoplankton generally and Ganf, 2000; Qui and Gao, 2002). Furthermore, some

stabilize or decrease while growth rates of many cyanobacteria cyanobacteria decrease cell division rates in response to lower

increase, providing a competitive advantage (Canale and Vogel, pH conditions (Shapiro and Wright, 1990; Whitton and Potts,

1974; Peperzak, 2003; Paerl and Huisman, 2009). 2000; Czerny et al., 2009). However, laboratory and ﬁeld studies

Beyond the direct effects on cyanobacterial growth rates, rising have demonstrated that other cyanobacteria respond to increased

temperatures will change many of the physical characteristics of CO2 with increased cell division rates, carbon ﬁxation, or both

aquatic environments in ways that may be favorable for cyano- (Hein and Sand-Jensen, 1997; Burkhardt et al., 1999; Hinga, 2002;

bacteria. For instance, higher temperatures will decrease surface Yang and Gao, 2003; Riebesell, 2004; Barcelos e Ramos et al., 2007;

water viscosity and increase nutrient diffusion towards the cell Fu et al., 2007, 2008; Hutchins et al., 2007; Levitan et al., 2007;

surface, an important process when competition for nutrients Riebesell et al., 2007; Kranz et al., 2009).

between species occurs (Vogel, 1996; Peperzak, 2003). Secondly, There are a number of phylogenetically distinct ways phyto-

since many cyanobacteria can regulate buoyancy to offset their plankton take up, transport, or convert CO2 and HCO3 (Raven,

sedimentation, a decrease in viscosity will preferentially promote 1997; Kaplan and Reinhold, 1999; Beardall and Giordano, 2002;

the sinking of larger, non-motile phytoplankton with weak Badger and Price, 2003; Reinfelder, 2011). Nearly all, eukaryotic

buoyancy regulation mechanisms (e.g. diatoms) giving cyanobac- algae and all cyanobacteria possess carbon-concentrating mecha-

teria a further advantage in these systems (Wagner and Adrian, nisms (CCMs; Giordano et al., 2005). Cyanobacteria have evolved

2009; Paerl and Huisman, 2009). Thirdly, insular heating will pathways for the active inorganic carbon uptake and partition their

increase the frequency, strength, and duration of stratiﬁcation. This ribulose bisphosphate carboxylase-oxygenase (Rubisco) into mi-

process will generally reduce the availability of nutrients in surface cro-compartments known as carboxysomes that generate a high

waters favoring cyanobacteria that regulate buoyancy to obtain concentration of CO2 around the Rubisco enzyme (Badger et al.,

nutrients from deeper water, or that are diazotrophic. Consistent 2002). It has been demonstrated that CCMs in cyanobacteria are

with the sum of these observations, cyanobacteria tend to dominate more efﬁcient than other algae or higher plants at low CO2

phytoplankton assemblages in eutrophic, freshwater environments concentrations (Badger and Price, 2003; Badger et al., 2006) and

during the warmest periods of the year, particularly in temperate that this heightened efﬁciency may facilitate their dominance

ecosystems (Paerl, 1988; Paerl et al., 2001; Paerl and Huisman, 2008; under low CO2 conditions (Price et al., 2008). Considered in the

Paul, 2008; Liu et al., 2011). For all of these reasons, it has generally context of climate change, increases in atmospheric concentrations

been concluded that cyanobacterial blooms may increase in of CO2 could have a more beneﬁcial impact on species that, unlike

distribution, duration and intensity, as global temperatures rise cyanobacteria, possess inferior CCMs, do not contain any CCMs,

(Paerl and Huisman, 2009; Paul, 2008). The precise response of and/or rely primarily on CO2 transport (Fu et al., 2007). While this

316 J.M. O’Neil et al. / Harmful Algae 14 (2012) 313–334

Fig. 1. Major CHAB genera from (A) freshwater: (1) Anabaena (photo: Michele Burford); (2) Microcystis (photo: Glenn MacGegor); (3) Cylindrospermopsis (photo: Glenn

MacGregor); (B) estuarine: (4) Nodularia (photo: Hans Paerl); (5) Aphanizomena (photo: Christina Esplund-Lindquist); (C) marine enivronments: (6) Lynbya (photo: Judy

O’Neil); (7) Trichodesmium (photo: Judy O’Neil); and (8) Synechococcus (photo: Florida Fish & Wildlife Institute-FWRI).

might suggest that globally rising CO2 may diminish the intensity As such, this review will focus on the role of eutrophication and

of cyanobacterial blooms, little is known regarding how increases climate change in the occurrence of three of the most prevalent

in the concentration of CO2 will impact cell physiology and growth pelagic cyanobacterial bloom forming genera in this environment,

rates of individual cyanobacteria genera. Changing CO2 conditions Anabaena, Microcystis, and Cylindrospermopsis (Fig. 1A).

may also effect the strain composition within a cyanobacterial

community. One study addressed this question using competition 3.1. Anabaena

experiments with toxic versus non-toxic strains of cyanobacteria

at high CO2 availability; which resulted in a competitive advantage Anabaena is a ubiquitous freshwater genus found throughout

of the non-toxic strain (Van de Waal et al., 2011). Below we will the world, but typically prevalent in lentic waterbodies such as

discuss what is known in regard to potential climate change effects lakes, reservoirs, cease-to-ﬂow rivers and weir pools. Anabaena is a

for each of the major harmful cyanobacterial bloom genera across ﬁlamentous, akinete-forming diazotroph in the order Nostocales.

the fresh to marine spectrum. Some species of this genera produce the toxins microcystins

(MCYs), anatoxin-a and anatoxin-a(S) and cylindrospermopsin

2.3.3. Salinity (CYN), while others, principally Anabaena circinalis, produces a

Climate change may also affect salinity in estuaries and saxitoxin (STX). The gene cluster responsible for anatoxin

freshwater systems due to rising sea-level: an increase in drought biosynthesis has recently been described for Anabaena (Rantala-

frequency and duration in some regions and concommittant Yilnen et al., 2011), the characterization of the gene clusters

increase in dessication; or in other areas, increases in precipitation responsible for saxitoxin biosynthesis (stx; Mihali et al., 2009) and

due to storms. This may cause shifts in phytoplankton species microcystin biosynthesis (mcyA – I; Rouhiainen et al., 2004) in

composition (Ahmed et al., 1985; Moisander et al., 2002; Bordalo Anabaena have allowed for the distinction between strains that can

and Vieira, 2005). Although many eukaryotic phytoplankton and cannot produce STX (Al-Tebrineh et al., 2010) and MCY

cannot tolerate changes in salinity, a number of cyanobacterial (Rouhiainen et al., 2004). As a diazotroph, Anabaena has been

species have very euryhaline tolerances. Therefore changes in functionally classiﬁed as tolerant of low nitrogen conditions, but

salinity may affect both community composition as well as sensitive to mixing and low light, utilizing buoyancy regulation to

potential toxin concentrations and distribution (Laamanen et al., counteract this sensitivity (Reynolds et al., 2002). Like a number of

2002; Orr et al., 2004; Tonk et al., 2007). other cyanobacterial genera, it is tolerant of low CO2 concentra-

tions, as it relies on the enzyme, carbonic anhydrase, to access

3. Freshwater environments bicarbonate (Shiraiwa and Miyachi, 1985). There are two main

HAB-forming species typically reported in the scientiﬁc literature –

As noted above, freshwater harmful algal blooms are predomi- A. circinalis and A. ﬂos-aquae. Recent studies of Anabaena have

nantly caused by pelagic cyanobacteria (Carmichael, 2001, 2008). focused principally on two main aspects: the life cycle; and the role

J.M. O’Neil et al. / Harmful Algae 14 (2012) 313–334 317

of physical conditions, namely light, stratiﬁcation, salinity and with the cyanobacteria Microcystis and Arthrospira (Giordanino

water ﬂow regimes in promoting growth. There have also been et al., 2011).

advances in the understanding of the life cycle of Anabaena, Flow conditions affect stratiﬁcation in cease-to-ﬂow river

particularly focused on factors causing akinete formation and systems, and therefore changes in rainfall patterns, and hence

germination (Tsujimura and Okubo, 2003; Karlsson-Elfgren and runoff to rivers, will have an impact on this. Studies have identiﬁed

Brunberg, 2004; Faithfull and Burns, 2006; Thompson et al., 2009). critical discharges to control A. circinalis blooms in the Barwon-

The role of nutrients, and the interaction with physical conditions, Darling River, Australia (Mitrovic et al., 2003, 2006). Researchers

has also received some attention. found that there was a 12% probability of A. circinalis blooms

À1

exceeding 15,000 cells mL under typical ﬂow conditions in the

3.1.1. Potential nutrient effects Murray River and threshold ﬂow rates were described to reduce

Anabaena is diazotrophic under low dissolved inorganic probability of blooms (Maier et al., 2004). Modeling studies of a

nitrogen conditions (Fogg, 1942). Many papers have examined thermally stratiﬁed reservoir with regular blooms of A. circinalis

this capacity in both ﬁeld and laboratory studies, and demonstrat- have shown that they can be controlled by the use of aerators or

ed that this physiological ability permits Anabaena to outcompete surface mixers (Lewis et al., 2004). Anabaena is purported to grow

non-nitrogen ﬁxers in N depauperate waters (e.g. Kangatharalin- in both fresh- and brackish waters and a recent study of Anabaena

gam et al., 1991; Chan et al., 2004; Wood et al., 2010) and even in ﬁeld experiments demonstrated that both growth and toxin

other diazotrophs such as Aphanizomenon (DeNobel et al., 1997). production were higher at lower salinity (Engstro¨m-O¨ st and

Since Anabaena is a diazotroph, P appears to be a key limiting Mikkonen, 2011). As such, higher ﬂow rates within river systems

nutrient for surface blooms of this genus. Limitation by P may also connected to estuaries may move Anabaena blooms into the

promote akinete production, a strategy for ensuring that popula- brackish portions of estuaries.

tions can recover when P becomes available again (Olli et al., 2005). These studies highlight the potential effect of climate change

Recently an agent-based model of the life cycle of Anabaena driven effects on rainfall patterns, and hence ﬂow regimes. In

determined that soon after germination, populations get most of southeast Australia, the combination of a predicted decrease in

their nutrients from the sediment bed (Hellweger et al., 2008). This rainfall coupled with increases in air temperature and evaporation

may give Anabaena a competitive advantage over other non- is modeled to give rise to measurable increases in Anabaena bloom

akinete forming genera, at least in the early stages of bloom occurrence and duration (Viney et al., 2007).

formation, until P becomes depleted or cells move into surface

waters. Furthermore, Rapala et al. (1997) found that both growth 3.2. Microcystis

rate and intracellular MCY concentrations of two Anabaena isolates

increased with increasing P concentrations. However, increases in Microcystis is one of the most common bloom formers in

DIN (e.g. nitrate) did not yield a signiﬁcant increase in growth rate freshwater systems on every continent except Antarctica

and had differing effects on the production of various microcystin (Fristachi and Sinclair, 2008). This genus can produce a suite of

congeners. An additional strategy available to Anabaena (and other potentially harmful compounds including MCYs, anatoxin-(a),

cyanobacterial species) is the ability to utilize organic forms of N and BMAA (Fristachi and Sinclair, 2008). Not all Microcystis cells

and P. Recently genes putatively encoding alkaline phosphatase produce MCY as bloom populations of Microcystis are typically

analogs have been identiﬁed in Anabaena (Luo et al., 2010). comprised of MCY-producing (MCY+) and non-MCY producing

(MCYÀ) strains that are distinguishable only via molecular

3.1.2. Potential climate change effects quantiﬁcation of the MCY synthetase gene operon (mcyA – J;

It has been proposed that increasing temperature will beneﬁt Tillett et al., 2000) and a molecular marker for the total

cyanobacteria, both directly and indirectly by increasing thermal Microcystis population, such as the 16S rRNA gene (Kurmayer

stratiﬁcation (Paerl and Huisman, 2008) and there is evidence and Kutzenberger, 2003; Davis et al., 2009). This method of

these processes will speciﬁcally promote Anabaena. Strong distinguishing between these sub-populations has been used in

stratiﬁcation that minimizes the availability of remineralized laboratory and ﬁeld studies during the past decade (e.g. Rinta-

nutrients in surface waters should favor diazotrophs such as Kanto et al., 2005; Davis et al., 2010; Van de Waal et al., 2011;

Anabaena and also speciﬁcally favors Anabaena physiology due to Wood et al., 2011). There is evidence that indicates that global

its ability to control buoyancy in the water column (Oliver, 1994). change to aquatic ecosystems such as rising temperatures,

Consistent with this concept, Brookes et al. (1999) reported that nutrient loads, and CO2 concentrations will affect the dominance

Anabaena forms blooms under thermally stratiﬁed conditions due and toxicity of Microcystis.

to the ability to regulate its buoyancy, and access sufﬁcient light for

growth and McCausland et al. (2005) speciﬁcally demonstrated 3.2.1. Potential nutrient effects

that stable conditions indicative of diurnal stratiﬁcation promote Historically, P has been considered the primary limiting

growth of A. circinalis. A recent study in a German lake showed that nutrient in freshwater ecosystems (Likens, 1972; Schindler,

Anabaena may beneﬁt from increased thermal stratiﬁcation as a 1977; Wetzel, 2001; Kalff, 2002; Paerl, 2008). There is evidence

result of temperature increases, although, this appeared to be to suggest, however, that N may be equally or more important than

linked to their ability to regulate their buoyancy and access P in the occurrence of toxic, non-diazotrophic cyanobacteria

nutrients in the hypolimnion rather than a direct temperature blooms, such as Microcystis. Laboratory studies have shown that

effect (Wagner and Adrian, 2009). Studies of A. circinalis popula- increasing N concentrations will generally increase the growth and

tions in the lower Murray River, Australia, exposed to persistent toxicity of Microcystis (Watanabe and Oishi, 1985; Codd and Poon,

stratiﬁcation were shown to grow faster than under diurnally 1988; Orr and Jones, 1998). Furthermore, experiments have

stratiﬁed or mixed conditions (Westwood and Ganf, 2004a). established positive relationships between DIN supply, MCY

Additionally, Westwood and Ganf (2004b) found that blooms were production, and MCY content in toxic strains of Microcystis

unlikely to form when periods of diurnal stratiﬁcation were less (Utkilen and Gjølme, 1995; Orr and Jones, 1998; Long et al.,

than 1 week. Finally, temperature will also have differential 2001). Field studies of Microcystis have also found that blooms are

physiological impacts on phytoplankton and a recent laboratory often associated with high levels of N (Jacoby et al., 2000; Gobler

study found that increasing water temperatures from 18 to 23 8C et al., 2007; Davis et al., 2010; Liu et al., 2011; Te and Gin, 2011;

increased Anabaena photosynthetic performance in comparison Paerl et al., 2011).

318 J.M. O’Neil et al. / Harmful Algae 14 (2012) 313–334

Nutrients can also differentially affect the relative abundance of blooms to P have been correlative ﬁeld studies which found MCY to

MCY+ and MCYÀ Microcystis strains. Laboratory experiments have be both positively and negatively correlated with various P pools

shown that MCYÀ strains of Microcystis require lower nutrient (Wicks and Thiel, 1990; Kotak et al., 1995; Lahti et al., 1997; Rinta-

concentrations to achieve maximal growth rates compared to Kanto et al., 2009). Recent ﬁeld studies in North America

MCY+ strains whereas MCY+ strains yield higher growth rates than examining MCY+ and MCYÀ strains of Microcystis suggest that

MCYÀ strains at high N concentrations (Ve´zie et al., 2002). MCY+ strains of Microcystis dominated the community during

Consistent with this trend, ﬁeld studies have shown that bloom times of elevated inorganic P (DIP) concentrations whereas MCYÀ

populations of Microcystis shifted from dominance of MCY+ strains strains became more abundant when DIP concentrations were

to MCYÀ strains as inorganic N concentrations declined through depleted (Davis et al., 2010). Consistent with this trend, MCY+

the summer (Davis et al., 2010). Several other studies have strains were enhanced by experimental P loading more frequently

observed a similar seasonal succession of Microcystis populations than MCYÀ strains (Davis et al., 2009, 2010). These ﬁndings

(Briand et al., 2004; Fastner et al., 2001; Welker et al., 2007) or have parallel the work of Ve´zie et al. (2002) who reported that the

noted the dominance of MCYÀ strains during the peak of growth rates of MCY+ Microcystis cultures exceeded MCYÀ strains

Microcystis bloom event (Welker et al., 2003, 2007; Kardinaal under high orthophosphate concentrations. Since some MCY+ have

et al., 2007). Since inorganic nutrient levels are generally reduced more light-harvesting pigments than MCYÀ strains (Hesse and

when algal blooms occur (Sunda et al., 2006), the predominance of Kohl, 2001), the RNA and DNA required for the synthesis of both

MCYÀ strains during this period may be a function of their ability light-harvesting pigments and microcystin by MCY+ strains may

to outcompete MCY+ strains when nutrient levels are lower (Ve´zie represent a signiﬁcant P requirement not present in MCYÀ strains.

et al., 2002). Consistent with this hypothesis, during ﬁeld-based, Recent genomic sequencing of two strains of Microcystis

incubation experiments, MCY+ strains were more frequently (Kaneko et al., 2007; Frangeul et al., 2008) has revealed an array

stimulated by higher concentrations of N than their MCYÀ of genes involved in the utilization of P including two high afﬁnity

counterparts (Davis et al., 2009, 2010). Microcystin is a N-rich phosphate binding proteins (pstS and sphX) and a putative alkaline

compound (10 N atoms per molecule) and studies have found that phosphatase (phoX). Subsequent sequence analyses among 10

microcystin can represent up to 2% of cellular dry weight of clones of M. aeruginosa has demonstrated that these genes are

Microcystis (Nagata et al., 1997). Additionally, toxic Microcystis present and conserved within the species and are strongly up-

strains have N requirements associated with the enzymes involved regulated (50–400-fold) by low DIP conditions (<2 mM) but not by

in the synthesis of MCY (Tillett et al., 2000) as well as with organic P sources (Harke et al., 2011). Since Microcystis dominates

additional light-harvesting pigments they may possess (Hesse and phytoplankton assemblages in summer when levels of DIP are

Kohl, 2001). Although the precise mechanism is unclear, toxic often low (Bertram, 1993; Wilhelm et al., 2003) and/or dominate

Microcystis cells seem to have a higher N requirement than non- lakes with low DIP and high organic P (Heath et al., 1995;

toxic cells (Ve´zie et al., 2002; Davis et al., 2010). Vanderploeg et al., 2001; Raikow et al., 2004), this species may rely

Studies have shown that some forms of DON can be utilized by on pstS, sphX, and phoX to efﬁciently transport DIP and exploit

Microcystis blooms. Field studies conducted by Takamura et al. organic sources of P to form blooms.

(1987) and Pre´sing et al. (2008) using N-labeled nitrogenous

compounds demonstrated that Microcystis was able to take up 3.2.2. Potential climate change effects

nitrate, ammonium, and urea. During a study of a New York lake Microcystis grows and photosynthesizes optimally at, or above,

where Microcystis represented more than 98% of the >20 mm 25 8C (Konopka and Brock, 1978; Takamura et al., 1985; Robarts

phytoplankton population, this size-fraction displayed ﬂexibility and Zohary, 1987; Reynolds, 2006; Jo¨hnk et al., 2008; Paerl and

in N assimilation, obtaining the majority of its N from nitrate, Huisman, 2008, 2009) and within an ecosystem setting, Microcystis

ammonium or urea on different occasions, as well as some of its N has been shown to out-compete species of eukaryotic algae at even

from glutamic acid (Davis, 2009). Uptake rates of ammonium and higher temperatures (30 8C; Fujimoto et al., 1997). Temperature

urea by the >20 mm size plankton community were signiﬁcantly effects on stratiﬁcation may further promote this genus. For

correlated with ambient concentrations of these nutrients example, like many bloom-forming cyanobacteria, Microcystis can

(P < 0.05) suggesting that N utilization by Microcystis was alter its position in the water column by regulating gas vesicle

dependent on nutrient availability. The >20 mm phytoplankton production (Walsby, 1975; Walsby et al., 1997) and negatively

group also obtained signiﬁcantly more of its total N from organic buoyant carbohydrate stores (Kromkamp and Walsby, 1990;

compounds than did smaller plankton (<20 mm), emphasizing the Visser et al., 1995, 1997). Since strong stratiﬁcation generally

importance of organic N as a source of nutrition for Microcystis. In favors the proliferation of buoyancy regulating cyanobacteria

support of this hypothesis, Berman and Chava (1999) found that (Kanoshina et al., 2003; Jacquet et al., 2005; Fernald et al., 2007;

non-axenic cultured Microcystis aeruginosa consistently grew best Jo¨hnk et al., 2008), increasing water temperatures that simulta-

using urea as a N source. Additionally, Dai et al. (2009) found that a neously increase stratiﬁcation will further promote the dominance

Chinese strain of M. aeruginosa was able to utilize amino acids, such of cyanobacteria such as Microcystis (Paerl and Huisman, 2009).

as alanine, leucine, and arginine to support growth and toxin Beyond stratiﬁcation, warmer temperatures also decrease water

production. Furthermore, genes associated with the uptake and viscosity, a change that may increase the sedimentation rate of

utilization of urea and amino acids have been identiﬁed in M. eukaryotic algae and further strengthen the competitive advantage

aeruginosa (Kaneko et al., 2007; Frangeul et al., 2008). Given that of Microcystis.

Microcystis can efﬁciently utilize both organic and inorganic Although theoretical studies have predicted that Microcystis and

species of N, successful bloom mitigation strategies will need to other bloom forming cyanobacteria will dominate under higher

target reductions in both N sources. temperatures, information regarding how subpopulations of

Phosphorus loading can favor the dominance of cyanobacteria Microcystis will be affected by changes in water temperature has

within phytoplankton communities (Fogg, 1969; Smith, 1986; been scarce. Davis et al. (2009) conducted surveys and temperature

Downing et al., 2001) and may also speciﬁcally promote the manipulation experiments in multiple ecosystems across the

density and/or toxicity of Microcystis. For example, Utkilen and temperate northeast USA and found that Microcystis became the

Gjølme (1995) found that an increase in P concentrations can lead dominant phytoplankton species present at all six study sites as

to an increase in MCY content of Microcystis cells. Until recently, temperatures reached their annual maximum. During ﬁeld-based

most ﬁeld work conducted relating the toxicity of cyanobacteria experiments, a 4 8C increase in temperatures yielded signiﬁcantly

J.M. O’Neil et al. / Harmful Algae 14 (2012) 313–334 319

higher growth rates for the MCY+ cells in most experiments, while Although, Cylindrospermopsis raciborskii can be found on almost

the growth rates of MCYÀ cells were enhanced by higher every continent, like most cyanobacterial bloom species the ability

temperature in only a third of experiments conducted (Davis to produce CYN is not universal. C. raciborskii has CYN producing

et al., 2009). Consistent with these trends, Kim et al. (2005) found (CYN+) and non-CYN producing (CYNÀ) strains identiﬁable by the

that toxic Microcystis strains cultured at 25 8C had more mcyB presence or absence of the CYN biosynthesis gene cluster (cyrA –

transcripts than cultures reared at 20 8C. Collectively these studies cyrO; Mihali et al., 2008). Lagos et al. (1999) found that Brazilian

suggest that higher temperatures not only promote Microcystis strains of C. raciborskii do not produce CYN although some strains

blooms but may favor the proliferation of MCY+ strains, and/or do produce the neurotoxin, saxitoxin. Also, previous studies have

strains with more MCY synthetase gene operons. found that European and Asian C. raciborskii strains can be toxic to

Changes in salinities due to changes in drought/storm cycles mice but do not contain any of the known cyanotoxins (Fastner

may affect Microcystis distribution and toxin production, since et al., 2003; Saker et al., 2003). While there have been accounts of

toxin production can increase with salinity. For instance, Micro- CYN being associated with systems containing Cylindrospermopsis

cystis PCC 7806 has high salt tolerance compared to most other in North America (Burns, 2008) and Italy (Messineo et al., 2010), no

freshwater phytoplankton (Tonk et al., 2007). This suggests that in North American or European strain has been found to produce CYN

freshwater ecosystems exposed to increasing salinity Microcystis or contain the CYN synthesis genes (Neilan et al., 2003; Kellmann

may gain an advantage over other phytoplankton species with et al., 2006; Yilmaz et al., 2008). Therefore, only Australian

lower salt tolerances and may become more toxic (Robson and (Hawkins et al., 1985; Ohtani et al., 1992), New Zealand (Wood and

Hamilton, 2003). Stirling, 2003) and some Asian (Li et al., 2001b; Chonudomkul et al.,

The impacts of rising CO2 concentrations on cyanobacterial 2004) strains of C. raciborskii have been found to produce CYN with

blooms is an area of research that has not, to date, been explored in Australian and New Zealand strains also producing the CYN

great detail and as described above, their precise response to these analogue, deoxy-cylindrospermopsin (Norris et al., 1999; Wood

conditions is uncertain. A recent study investigating the impacts of and Stirling, 2003).

increased CO2 concentrations on competition between MCY+ and

MCYÀ strains of Microcystis found MCY+ strains dominated at low 3.3.1. Potential nutrient effects

CO2 concentrations, whereas MCYÀ strains were more abundant C. raciborskii is a diazotroph, but low DIN conditions are not a

under elevated CO2 concentrations (Van de Waal et al., 2011). The prerequisite for blooms. A microcosm experiment examined the

authors note that prior studies have found that MCYs could play a competition between C. raciborskii and another diazotroph,

role in the acquisition of CO2 at low concentrations (Ja¨hnichen Anabaena spp. found that C. raciborskii was a stronger competitor

et al., 2001, 2007). Furthermore, another study found elevated for DIN than Anabaena (Moisander et al., 2008). Studies have

concentrations of MCYs in the carboxysomes of cyanobacteria shown that under DIN replete conditions, DIN uptake rates were

(Gerbersdorf, 2006). Given that previous research has demon- higher than N ﬁxation rates for C. raciborskii-dominated waters

strated that elevated temperature favors MCY+ Microcystis strains (Pre´sing et al., 1996; Burford et al., 2006). Since diazotrophy is an

(Davis et al., 2009) the response of this harmful cyanobacterial energetically costly biochemical process, it is not surprising that

bloom species to future climate change scenarios that include ammonium is preferentially used, when available. Laboratory

temperature and CO2 concentrations is difﬁcult to predict. Further studies have conﬁrmed that C. raciborskii growth rates were fastest

research into the response of Microcystis to changes in CO2 when N was supplied as ammonium, followed by nitrate, then urea

concentrations alone, and in conjunction with other global change (Saker et al., 1999; Hawkins et al., 2001; Saker and Neilan, 2001). It

parameters, is needed to better understand these interactions. has been proposed that activation of N2-ﬁxation was dependent on

the N content of the cells (Spro˝ ber et al., 2003). Therefore, C.

3.3. Cylindrospermopsis raciborskii seems to display a ﬂexible N strategy: when DIN

concentrations are sufﬁcient, this source is used, and during

The cyanobacterium Cylindrospermopsis is a solitary, ﬁlamen- periods of depletion, N2-ﬁxation is employed.

tous diazotroph. It was once thought to be a strictly tropical/ Little is known about the effect of N on CYN production. Several

subtropical species being ﬁrst identiﬁed in Java in 1912 studies have investigated the impact of different sources of DIN on

(Koma´rkova´, 1998). In the past decade there has been a substantial CYN content of Australian isolates of C. raciborskii and found that

expansion in its geographical range across every continent, except the highest intracellular CYN content (reported as % of freeze-dried

Antarctica: Australia/Oceania (Hawkins et al., 1985; Wood and weight) were in the cultures devoid of a ﬁxed N source and lowest

Stirling, 2003), North America (Chapman and Schelske, 1997; in cultures grown with saturating concentrations of ammonium

Hamilton et al., 2005; Hong et al., 2006), South America (Branco (Saker et al., 1999; Saker, 2000; Saker and Neilan, 2001). This

and Senna, 1996; Bouvy et al., 2006; Figueredo and Giani, 2009), contrasts with patterns of growth rates that were highest in the

Europe (Fastner et al., 2003; Saker et al., 2003; Briand et al., 2004; presence of ammonium and the lowest in the absence of a ﬁxed N

Monteiro et al., 2011), Africa (Dufour et al., 2006; Mohamed, 2007) source (Saker et al., 1999; Saker and Neilan, 2001). Mihali et al.

and Asia (Chonudomkul et al., 2004). Cylindrospermopsis was ﬁrst (2008) hypothesized that increased intracellular CYN content in

deemed a harmful bloom species after a toxic bloom event in 1979 the absence of ﬁxed N was due to the ﬂanking of the CYN

caused acute hepato-enteritis and renal damage among more than biosynthesis gene cluster in the C. raciborskii genome by hyp gene

150 people on Palm Island, off the coast of North Queensland, homologs associated with the maturation of hydrogenases. Since

Australia (Hawkins et al., 1985; Carmichael, 2001). The structure of the hyp gene cluster is controlled by the global N regulator (ntcA;

cylindrospermosin (CYN), the toxin responsible, was determined activates the transcription of the N assimilation genes) in another

in 1992 (Ohtani et al., 1992), when the mystery of the so-called cyanobacterium, Nostoc sp. strain PCC73102, it is plausible that the

‘‘Palm Island disease’’ was resolved (Grifﬁths and Saker, 2003). hyp genes and, therefore, the CYN biosynthesis gene cluster are

Subsequently, it has been shown that other cyanobacteria under the same regulation in C. raciborskii (Mihali et al., 2008).

including Umezakia natans (Harada et al., 1994), Aphanizomenon Phosphorus appears to play an important role in the dominance

ovalisporum (Shaw et al., 1999; Carmichael, 2001), Lyngbya wollei of, and CYN production by, C. raciborskii. This species blooms in

(Seifert et al., 2007), Raphidiopsis mediterraena (McGregor et al., reservoirs and lakes when phosphate concentrations are below

2011), and Anabaena lapponica (Spoof et al., 2006) also are capable detection limits (Padisa´k and Istvanovics, 1997; Burford and

of producing CYN. O’Donohue, 2006). Istva`novics et al. (2000) showed that a

320 J.M. O’Neil et al. / Harmful Algae 14 (2012) 313–334

European strain of C. raciborskii had a high P afﬁnity and storage raciborskii. C. raciborskii often blooms in stratiﬁed, deeper

capacity, and consistent with this ﬁnding, ﬁeld studies have reservoirs (>15 m) (McGregor and Fabbro, 2000). Severe blooms

concluded C. raciborskii dominance may be related to its superior of C. raciborskii occurred in a subtropical reservoir during periods of

DIP scavenging ability under stratiﬁed, low DIP concentrations low rainfall, and when the water column was more stable (Harris

(Padisa´k, 1997; Shaﬁk et al., 2001; Antenucci et al., 2005; Posselt and Baxter, 1996). It was concluded that vertical stratiﬁcation

et al., 2009). Furthermore, a recent laboratory study showed that C. provided a competitive advantage for C. raciborskii over other algal

raciborskii grows faster under P limitation when there is sufﬁcient species likely due to its superior DIP scavenging ability under

supply of DIN (Kenesi et al., 2009). Other studies have found that stratiﬁed, low DIP concentrations (Antenucci et al., 2005; Burford

CYN concentrations have been positively correlated with total P and O’Donohue, 2006). Interestingly, the installation of a

concentrations (Wiedner et al., 2008) and that CYN production destratiﬁcation unit in this reservoir designed to reduce stratiﬁca-

rates are positively correlated with C. raciborskii growth rates in P- tion did not mitigate C. raciborskii blooms but rather yielded earlier

limited cultures during exponential growth (P. Orr, personal bloom initiation and a longer persistence of blooms (Antenucci

communication). In a manner similar to Microcystis, the recent et al., 2005; Burford and O’Donohue, 2006). This is likely due to the

sequencing of an Australian strain of C. raciborskii (Stucken et al., ability of cells to photoadapt to dark and ﬂuctuating light

2010) allowed for identiﬁcation of genes associated with P uptake conditions (O’Brien et al., 2009). Laboratory studies have shown

and utilization that may be related to its ability to persist under that C. raciborskii has low light requirements for optimal growth

low P conditions. C. raciborskii contains the genes to utilize (Shaﬁk et al., 2001; Briand et al., 2004; Dyble et al., 2006).

inorganic and organic P including high afﬁnity phosphate binding Consistent with this ﬁnding, C. raciborskii, is not positively buoyant,

proteins (pstS, sphX), phosphanate uptake (phnC,D,E) and metabo- but does have very low rates of sinking (Kehoe, 2010). Collectively,

lism (phnG-M,X,W), and phosphorus ester metabolism (phoA). In these ﬁndings suggest strong stratiﬁcation is not a requisite

laboratory cultures, C. raciborskii has been shown to utilize DOP, condition for C. raciborskii blooms.

giving it an advantage over algae that do not utilize this P source in

low DIP environments (Posselt, 2009). 4. Estuarine environments

3.3.2. Potential climate change effects There are several genera of euryhaline cyanobacteria that

The growth response of C. raciborskii to temperature has been bloom in estuarine environments with a range of salinities (Paerl,

examined using multiple strains isolated from both temperate and 1988; Stal and Zehr, 2008). The site of perhaps the most widely

tropical areas (Briand et al., 2004; Chonudomkul et al., 2004). In studied estuarine cyanobacterial blooms is the Baltic Sea, one of

studies of subtropical and tropical reservoirs in Australia, C. the largest brackish water bodies in the world. This system has

raciborskii was found to be chronically dominant in tropical been experiencing an acceleration of anthropogenic nutrient

reservoirs, but only bloomed during summer in the subtropics inputs from a densely populated (80 million people) watershed

(Bouvy et al., 2000; McGregor and Fabbro, 2000; Burford and in recent decades (Larsson et al., 1985; Elmgren, 2001). Blooms of

O’Donohue, 2006; Burford et al., 2007). Studies have also found diazotrophic cyanobacteria are common during the summer

that C. raciborskii dominates temperate systems at higher months in the Baltic (Edler, 1979; Stal et al., 2003) sometimes

temperatures (i.e. summer months; Hamilton et al., 2005; Conroy covering >100,000 km (Kahru, 1997). It has been hypothesized

et al., 2007). C. raciborskii displays positive net growth from 20 to that these blooms have been regular features of this ecosystem

35 8C, with maximum rates at 30 8C (Saker and Grifﬁths, 2000). since 7000 years before present, when the Baltic Sea ﬁrst became a

This temperature tolerance explains the capacity of C. raciborskii to brackish water body (Bianchi et al., 2000). In contrast, Zille´n and

invade both temperate and tropical areas of the world as well as its Conley (2010) argue that the Baltic Sea did not experience these

seasonality in sub-tropical and temperate ecosystems (e.g. events until the recent emergence of anthropogenic P loading and

Chapman and Schelske, 1997; Fastner et al., 2003; Briand et al., deep water hypoxia during summer. Regardless, cyanobacterial

2004; Hong et al., 2006; Messineo et al., 2010). It has been blooms have been documented in all basins of the central Baltic Sea

proposed that cyanobacteria will increasingly dominate freshwa- and in the Gulf of Finland (Karjalainen et al., 2007) and are

ter systems due to global warming (Padisa´k, 1997; Paerl and becoming more frequent and intense in most areas (Kahru et al.,

Huisman, 2008) and the high temperature optima for maximal 1994; Finni et al., 2001; Poutanen and Nikkila¨, 2001; Mazur-

growth in C. raciborskii indicates this species is one of the most Marzec et al., 2006) including the Bothnian Sea where, until

likely cyanobacteria to beneﬁt from climatic warming. Consistent recently, these events had been rare (Niemi, 1979; Kahru et al.,

with this hypothesis, Wiedner et al. (2007) has shown that growth 1994).

initiation of C. raciborskii is controlled by temperature in German The three primary bloom-forming cyanobacterial genera in the

lakes and has proposed that the invasion of C. raciborskii into these Baltic Sea are Nodularia, Aphanizomenon, and Anabaena (Fig. 1B).

lakes is the result of global climate change. The sole producer of cyanotoxins in the Baltic was thought to be

Temperature has been found to play a key role in the production Nodularia as Aphanizomenon had been reported to be non-toxic

of CYN, although there seems to be a ‘‘disconnect’’ between (Sivonen et al., 1989; Repka et al., 2004). Karlsson et al. (2005)

optimal growth temperature and optimal CYN production suspected that Anabaena produced MCYs and recent studies have

temperature for C. raciborskii. Saker and Grifﬁths (2000) found conﬁrmed this (Halinen et al., 2007). Since Anabaena has been

that cell toxicity was highest at 20 8C, but that optimal growth discussed above and since Nodularia spp., which produces the

occurred between 25 and 30 8C. Moreover, they found a negative hepatotoxin nodularin, is the main toxin producing and best-

correlation between temperature and CYN production between 20 studied cyanobacterium found in this system, this review will

and 35 8C with no CYN production at 35 8C despite continued focus primarily on the impacts of continued eutrophication and

growth at this temperature. This and other studies suggest that climatic change on this cyanobacterium but will also consider

although maximum C. raciborskii growth rates occur at higher competition between this genera and Aphanizomenon.

temperatures (25–35 8C; Saker and Grifﬁths, 2000; Briand et al.,

2004), these temperatures produce cells with lower CYN content. 4.1. Nodularia

Although it has been hypothesized that enhanced stratiﬁcation

will lead to more sustained cyanobacterial blooms (Paerl and Nodularia spp. blooms occur in brackish waters worldwide

Huisman, 2008, 2009), this hypothesis may be less applicable to C. (Sellner, 1997; Bolch et al., 1999; Moisander and Pearl, 2000) and

J.M. O’Neil et al. / Harmful Algae 14 (2012) 313–334 321

N. spumigena was the species responsible for the ﬁrst well Nodularia seemed to grow well at a range of P concentrations

documented bloom of a toxic cyanobacterial species in the world (Vahtera et al., 2007). This may be due to Nodularia’s ability to

(Francis, 1878). Komarek et al. (1993) differentiated strains of rapidly utilize pulses of P as well as a high P storage capacity (Mur

Nodularia from the Baltic Sea by multiple ecological and et al., 1999; Vahtera et al., 2007) although this has been debated

morphological factors including the presence of gas vesicles, the (Larsson et al., 2001; Kangro et al., 2007). Collectively, these

dimensions and shapes of vegetative cells, heterocytes, akinetes, ﬁndings suggest management plans aimed towards reducing P

and the size and shape of trichomes. However, it was later shown loads may favor a shift in dominance among cyanobacteria from

that morphological features did not accurately differentiate Aphanizomenon to Nodularia.

Nodularia strains in the Baltic (Barker et al., 1999). It is currently Like most microbes, Nodularia can produce alkaline phosphatase

believed that there are only three species of Nodularia in the Baltic (APase) to utilize the monophosphate esters when orthophosphate

Sea, one planktonic, N. spumigena, and two benthic (N. sphaer- is depleted. Nodularia is well-adapted to take advantage of organic P

ocarpa and N. harveyana; Laamanen et al., 2001; Janson and as it has a lower substrate half-saturation constants (KM) and higher

Grane´li, 2002; Lyra et al., 2005). The latter two are relatively Vmax:KM ratio of the APase enzyme than Aphanizomenon suggesting

uncommon and found only in coastal habitats (Lyra et al., 2005). it has a higher afﬁnity for organic P (Degerholm et al., 2006).

Nodularia spumigena produces nodularin (NOD), which can have Compared to other phytoplankton in the Baltic, N. spumigena

severe negative impacts when ingested by terrestrial vertebrates populations had a higher percentage of cells displaying APase

(Rinehart et al., 1988; Runnegar et al., 1988; Eriksson et al., 1990) activity and were superior competitors for DOP (Vahtera et al.,

including the promotion of liver tumors and acts directly as a liver 2010). The ability of Nodularia to efﬁciently utilize DOP is consistent

carcinogen (Carmichael et al., 1988; Sivonen et al., 1989), due to with the hypothesis that reductions in DIP may promote a

inhibition of protein phosphatases (Ohta et al., 1994). Nodularin succession of cyanobacterial communities towards this genus.

can compromise up to 2% of cellular dry weight of N. spumigena Availability of phosphorus has been shown to affect NOD

(Komarek et al., 1993). production in Nodularia. Expression of the nda gene cluster

Similar to many cyanotoxins, NOD is synthesized non- increased in response to DIP starvation (Jonasson et al., 2008)

ribosomally by a multifunctional enzyme complex consisting of but measurements of intracellular and extracellular NOD indicated

both peptide synthetase and polyketide synthase modules as well that levels did not vary signiﬁcantly with P depletion (Repka et al.,

as tailoring enzymes (ndaA – I; Mofﬁtt and Neilan, 2004). 2001; Jonasson et al., 2008), suggesting the existence of a post-

Koskenniemi et al. (2007) developed a qPCR assay for Nodularia transcriptional control of NOD production. Interestingly, Lehtima¨ki

spp. and found that ndaF gene copies were strongly correlated with et al. (1994, 1997) reported that high P concentration yielded

NOD concentrations in the Baltic Sea, a ﬁnding that parallels those higher NOD production while Repka et al. (2001) found that

for Microcystis, MCY, and the mcyD gene in North America (Davis Nodularia biomass increased with increasing P while NOD

et al., 2009, 2010). N. spumigena is the only known NOD-producing, concentrations did not. Lastly, Lehtima¨ki et al. (1994) found that

bloom-forming Nodularia species in the Baltic Sea (Sivonen et al., NODÀ strains of Nodularia grew better than NOD+ strains at low P

1989; Kononen et al., 1996; Stal et al., 2003; Kru¨ ger et al., 2009). In concentrations which suggests that, in a manner similar to

this section we discuss the potential impacts of eutrophication and Microcystis, synthesis of this hepatoxin represents an additional

climate change on the growth and NOD production of Nodularia P burden for NOD+ cells (Ve´zie et al., 2002; Davis et al., 2009, 2010).

spp. in general, and N. spumigena, in particular. Clearly, the role of P in NOD production is not yet fully understood.

Marine primary production is generally considered to be N

4.1.1. Nutrients limited (Paerl, 1988) and since Nodularia spp. are diazotrophic,

Eutrophication and resulting hypoxia associated with stratiﬁ- their dynamics are controlled primarily by temperature, salinity

cation strongly inﬂuence the ecology of the Baltic Sea ecosystem and P (Grane´li et al., 1990; Plinski and Jo´ zwiak, 1999; Stal et al.,

(HELCOM, 2007). Over geological time, prolonged periods of 2003) but not N. Supporting this view, Vuorio et al. (2005) found

hypoxia in the Baltic Sea have paralleled warmer climatic that N. spumigena biomass decreased with increased ﬁxed N

conditions (Zille´n et al., 2008). Hypoxia enhances P ﬂuxes from concentrations while Jonasson et al. (2008) found the expression of

sediments, decreasing N:P ratios and favoring blooms of diazo- the nda gene cluster decreased with increasing ammonium

trophic cyanobacteria (Vahtera et al., 2007). Continued increases in concentrations. Conversely, when ammonium concentrations

global temperatures are likely to promote longer periods of were low, NDA synthesis genes, as well as N2-ﬁxation genes, were

stratiﬁcation and hypoxia and, increased ﬂuxes of N and P from upregulated (Jonasson et al., 2008). Vintila and El-Shehawy (2010)

sediments (Wulff et al., 2007). As described below, this could lead concluded that Baltic strains of N. spumigena are not efﬁcient at

to more prolonged and intense cyanobacterial blooms in the Baltic. utilizing DIN. Consistent with these ﬁndings, stratiﬁed conditions

Availability of phosphorus affects the spatial and temporal induced by the late summer water temperatures lead to N

distribution of cyanobacteria in the Baltic Sea (Niemi, 1979). depletion (low DIN:DIP ratios) and favored the growth of

Summer stratiﬁcation promotes hypoxia, P-ﬂuxes, and, as a diazotrophic cyanobacteria such as Nodularia spp. (Niemi, 1979;

consequence, blooms of diazotrophic cyanobacteria in the Baltic Kononen et al., 1996; Stal et al., 1999).

(Fonselius, 1978; Lindahl et al., 1980; Stockner and Shortreed,

1988). Furthermore, in shallower areas of the Baltic Sea, wind- 4.1.2. Potental climate change effects

driven re-suspension of P from bottom sediments (Blomqvist and Studies have found that Nodularia spp. typically grows

Larsson, 1994; Heiskanen and Leppa¨nen, 1995) as well as P from optimally at temperatures between 20 and 25 8C (Lehtima¨ki

terrestrial sources and river discharge (Stepanauskas et al., 2000, et al., 1994, 1997), whereas its primary cyanobacterial competitor,

2002) may facilitate bloom formation. Of the three primary bloom Aphanizomenon spp., grows faster at lower temperatures (16–

forming cyanobacteria in the Baltic, Nodularia appears to be best 22 8C; Lehtima¨ki et al., 1994, 1997). High temperatures (25–30 8C)

adapted to low-P conditions (Uehlinger, 1981; Wallstro¨m et al., promoted the growth and NDA production by NDA+ Nodularia spp.

1992; DeNobel et al., 1997), whereas Aphanizomenon may be a (Lehtima¨ki et al., 1997; Hobson and Fallowﬁeld, 2003), whereas

better competitor for higher levels of available P (Wallstro¨m, 1988; NDAÀ strains of Nodularia grew better than NDA+ strains at lower

Gro¨nlund et al., 1996; Kononen et al., 1996; Kononen and temperatures (Lehtima¨ki et al., 1994). Therefore, continued

Leppa¨nen, 1997). Another study found that Aphanizomenon climatic warming will likely promote greater abundances and

populations were dependent on ample P concentrations; whereas toxin synthesis by NDA+ Nodularia populations in the Baltic Sea.

322 J.M. O’Neil et al. / Harmful Algae 14 (2012) 313–334

To date, there has only been a single investigation of the effects (Koma´ rek and Golubic, 2005; Koma´ rek, 2006; Engene et al.,

of increasing CO2 on Nodularia spp. Czerny et al. (2009) found that 2011a).The ambiguity of Lyngbya taxonomy and inherent

N. spumigena exposed to higher CO2 concentrations displayed problems in morphological identiﬁcation are highlighted in

reduced cell division rates and N2-ﬁxation rates and hypothesized recent work by Jones et al. (2011) who have sequenced the

that N. spumigena is well-adapted to the low CO2/high pH genome of L. majuscula ‘‘3D’’, which has been in culture for 15

conditions that develop during dense blooms in the poorly years, and was originally isolated from Curacao. In addition to

buffered brackish Baltic (Thomas and Schneider, 1999). This ﬁnding a complex network of genes that suggests an enhanced

hypothesis is consistent with several other studies that reported ability to adapt to shifting conditions in dynamic coastal marine

cyanobacteria can out-compete eukaryotic algae under high pH environments, this study also had the surprising result of not

and low CO2 conditions (Shapiro and Wright, 1990; Oliver and ﬁnding nif genes for N2 ﬁxation, despite multiple studies of this

Ganf, 2000). Hence, rising CO2 concentrations may reduce the species across the world reporting it as being diazotrophic (Jones,

severity of N. spumigena blooms by causing a shift in dominance to 1990; Dennison et al., 1999; Lundgren et al., 2003; Elmetri and

species that are positively affected by the increased CO2 Bell, 2004; O’Neil and Dennison, 2005). Additionally, other

concentrations. Given the scarcity of research on this topic and researchers have speciﬁcally identiﬁed nif genes in L. majuscula

that expected higher temperatures will favor the growth of N. (Joyner et al., 2008). It has been suggested that this may reﬂect

spumigena (see above) further research is required to better ‘‘strain differences’’ (Engene et al., 2010) or co-mingling of

understand the possible trajectories of this genera in the face of different cyanobacteria or mis-identiﬁcation of similar looking

climate change. cyanobacteria (Jones et al., 2011). Clearly, this illustrates the need

for better understanding of cyanobacteria taxonomy and reﬁning

5. Marine environment of techniques to match morphological and molecular identiﬁca-

tions (Engene et al., 2011a, 2011b).

The prevalence of cyanobacterial blooms in aquatic environ- The toxins produced by Lyngbya spp. seem to vary signiﬁcantly

ments generally follows the hierarchy of freshwater > estuarine/ not only by geographic location, but by environmental conditions

brackish > marine systems (Fristachi and Sinclair, 2008). Dino- and growth stage (Osborne et al., 2001; Capper et al., 2006). The

ﬂagellates have often been the more commonly studied marine fresh water species L. wollei is capable of producing saxitoxin

HAB, possibly due in part to their acute effects on human health (Onodera et al., 1997; Mihali et al., 2011) as well as cylindros-

(Yasumoto and Murata, 1993; Wang, 2008). In contrast, the permopsin (Seifert et al., 2007). L. majuscula, the most commonly

harmful effects of marine cyanobacteria may be subtler and/or reported marine species, is found mainly in tropical waters and

more chronic (e.g., BMAA). The most conspicuous marine produces several demotoxic alkaloids, neurotoxins, as well as a

cyanobacterial bloom formers that will be the foci of this review plethora of bioactive compounds with natural product uses

are ﬁlamentous, colonial members of the genera Lyngbya, and (Osborne et al., 2001; Nogle and Gerwick, 2002; Gerwick et al.,

Trichodesmium and the coccoid cyanobacteria Synechococcus 2008; Tan, 2007; Jones et al., 2011; Engene et al., 2011a), with 50

(Fig. 1C). new bioactive peptides reported since 2007 alone (Liu and Rein,

2010). The sheer number of natural products isolated from the

5.1. Lyngbya species L. majuscula alone, has prompted a re-examination of this

genus and there are taxonomic reassignments that have currently

Cyanobacteria of the genus Lyngbya are generally benthic been proposed (Engene et al., 2011a,b).

species growing attached to seagrasses, macroalgae, corals and There have been several detailed reviews of toxins associated

sediment. They also can form dense surface blooms when with L. majuscula (Moore, 1981; Osborne et al., 2001) which

they episodically detach from their benthic substrates buoyed include Lyngbyatoxin-A (LTA), and debromoaplysiatoxin (DTA).

by gas vesicles and bubbles trapped within their ﬁlaments after Deleterious effects of these compounds include asthma-like

active photosynthesis, especially under calm stratiﬁed condi- symptoms and severe dermatitis in humans (Osborne et al.,

tions. This acts as a means of dispersal, and can also cause 2001, 2007). These compounds have also been implicated in tumor

serious economic and health issues when blooms wash up on promotion in green sea turtles which may ingest L. majuscula

beaches necessitating cleanup of rotting, malodorous biomass growing epiphytically on seagrasses (Arthur et al., 2006, 2008).

(Watkinson et al., 2005; Albert et al., 2005; O’Neil and Dennison, Additionally, one human fatality has been attributed to the

2005). presence of LTA in ingested green turtle meat (Yasumoto, 1998).

Lyngbya occur in many environments along the fresh to More recently new microcolins, lyngbyamides and barbamides

marine continuum with over 70 species described (Cronberg (see review Liu et al., 2011) have been identiﬁed in addition to

et al., 2003). The two most commonly reported bloom species are previously reported bioactive deterrents to ﬁsh and invertebrate

the freshwater/to brackish species L. wollei and the marine grazing (Pennings et al., 1996; Nagle et al., 1998; Capper et al.,

species Lyngbya majuscula, Lyngbya confervoides, Lyngbya poly- 2005, 2006; Capper and Paul, 2008).

chroa (Paerl et al., 2008; Sharp et al., 2009), and Lyngbya bouillonii Blooms of L. majuscula were ﬁrst reported as toxic in Hawaii,

(Hoffmann and Demoulin, 1991; Hoffmann, 1999) have also been USA, in the 1950s through the1970s (Banner, 1959; Moikeha and

reported to often grow over corals (Paul et al., 2005). Recently, Chu, 1971; Hashimoto et al., 1976). Large blooms have been

the lesser known freshwater species Lyngbya hieronymusii and/or reported since the late 1990s in several locations in Australia, most

Lyngbya robusta have been forming blooms in Lake Atitlan, severely in Moreton Bay, Queensland off the coast of the city of

Guatamala (Rejma´ nkova´ et al., 2011). Cyanobacteria taxonomy is Brisbane, resulting in severe dermatitis and asthma-like symptoms

often imprecise, particularly in the case of the polyphyletic in ﬁsherman (Dennison et al., 1999; Watkinson et al., 2005; Albert

characteristics of the Lyngbya genera (Speziale and Dyck, 1992; et al., 2005; O’Neil and Dennison, 2005). Blooms have also been

Engene et al., 2011a, 2011b), and while improvements in reported in more pristine locations such as Shoalwater Bay,

classiﬁcation have been made (Anagnostidis and Koma´ rek, Queensland (Arthur et al., 2006), and on the Great Barrier Reef, at

1985, 1988, 1990; Koma´ rek and Anagnostidis, 1989, 2005), Hardy Reef (Albert et al., 2005). Most recently, blooms have been

including the recent reclassiﬁcation of some Lyngbya species to occurring in various locations in Western Australia in the Peel-

the genus Moorea (Engene et al., 2011b), it is clear molecular Harvey Estuary near Perth and in Roebuck Bay, near Broome

analyses are necessary, and will assist in reclassiﬁcations (Deeley, 2009) as well as in the Northern Territory in Darwin

J.M. O’Neil et al. / Harmful Algae 14 (2012) 313–334 323

Harbour (Drewry et al., 2010). Potential causes include increased 5.1.2. Potential climate change effects

nutrient input from groundwater (Environmental Protection L. majuscula occurs in tropical and sub-tropical environments

Authority, 2008) and tidal creeks (Drewry et al., 2010). Blooms and grows at maximal rates between 24 and 30 8C (Watkinson

have also been reported in various locations in Florida (Paerl et al., et al., 2005). The high temperature requirements for L. majuscula

2008; Paul et al., 2005; Sharp et al., 2009). The Caribbean and the are similar to those reported for other cyanobacteria (Robarts

South Paciﬁc have been active spots for Lyngbya isolates for natural and Zohary, 1987; Paul, 2008; Paerl and Huisman, 2008, 2009).

products chemistry (e.g. Tan, 2007, 2010; Gerwick et al., 2008; Projected temperature increases this century (IPCC, 2007) may

Engene et al., 2011a). increase the bloom persistence and duration of L. majuscula

where they already occur, as well as increase its geographic

5.1.1. Potential effects of nutrients range. This has already been observed in Moreton Bay, where

Many Lyngbya species are reportedly diazotrophs (Jones, 1990; small populations of L. majuscula now persist through winter

Dennison et al., 1999; Elmetri and Bell, 2004; Lundgren et al., 2003; months (C. Roelfsema UQ, personal communication). Its northern

cf. Jones et al., 2011), ﬁxing dinitrogen mainly at night. However, it range on the East Coast of the US may be expanding with

appears to be very ﬂexible in its N acquisition strategies, and can extensive blooms during summer months observed recently in

grow on inorganic as well as organic (urea) forms of N (O’Neil et al., Provincetown Massachusetts (J.M. O’Neil, personal observation.)

2004), similar to other diazotrophic cyanobacteria such as and Penobscott Bay Maine (K.A. Studholme UMCES, personal

Cylindrospermopsis. Also, similar to other diazotrophs, Lyngbya communication).

growth and productivity is often stimulated by P (Elmetri and Bell, Beyond affecting growth, temperature and physical factors in

2004; Watkinson et al., 2005; Ahern et al., 2006a, 2008). In addition the environments where blooms occur, may also inﬂuence

to taking up nutrients from the water column, its benthic habitat secondary metabolite accumulation in cyanobacteria. (Watanabe

permits utilization of redox-based, diel phosphorus and iron ﬂuxes and Oishi, 1985; Sivonen, 1990; Rapala et al., 1997; Lehtima¨ki

from sediments at night when ﬁxation is at maximal capacity et al., 1994; Paul, 2008). While temperature has not been directly

(Watkinson et al., 2005). Ammonium ﬂuxes from the sediments are linked to increased toxin production in L. majuscula, maximum

also observed at night, and given the ﬂexible physiology of L. toxin concentrations typically occur at the peak of bloom

majuscula, it may switch between the most energetically efﬁcient abundances that often coincide with temperature and growth

N source, ammonium, and N ﬁxation, depending on availability maxima (Osborne, 2004). Given that bloom initiation of L.

(O’Neil et al., 2004; Paerl et al., 2008). majuscula is in the benthos, periods of higher temperatures and

Blooms of L. majuscula have increased in abundance, severity, water column stability, coincide with higher benthic light

and duration in tropical and subtropical regions around the globe penetration and thus increase growth and productivity for L.

in the past several decades and in many instances blooms have majuscula (Watkinson et al., 2005). These changes may also

been linked to anthropogenic eutrophication. In Australia, for directly or indirectly change other physiological features such as

example, L. majuscula had not been a conspicuous bloom former in toxin production. For instance, it has been demonstrated that

35 years of nearly daily observation on Hardy Reef, located offshore concentrations of the bioactive compound pitipeptolide A in L.

of the Whitsunday Islands along the Great Barrier Reef. However, L. majuscula increase under high light levels (Pangilinan, 2000, as

majuscula began overgrowing branching corals, and benthic cited in Paul, 2008). To date, no study has examined the effects of

calcareous macroalgal species (e.g., Udotea; Penicillus) a few increasing CO2 on Lyngbya.

months after the installation of a tourist helicopter platform in

the reef lagoon (Albert et al., 2005). The platform became a roost 5.2. Trichodesmium

for hundreds of sea-birds, causing a concentrated source of guano-

derived N and P, pooling at low tide, and it was hypothesized that Trichodesmium a colonial non-heterocystous ﬁlamentous mem-

this was stimulating L. majuscula productivity (Albert et al., 2005). ber of the Oscillatoriales, is the most abundant bloom forming

Similarly, a lesser known freshwater species, L. robusta, began cyanobacteria in the marine pelagic environment with a pan-

forming blooms in Lake Atitlan, Guatemala in 2008 after years of global distribution in oligotrophic waters of tropical and subtropi-

sustained nutrient inputs and increased runoff from tropical storm cal oceans (Capone et al., 1997; LaRoche and Breitbarth, 2005).

activity that increased P levels and decreased N:P ratios Blooms generally occur in stable clear water columns with low

(Rejma´nkova´ et al., 2011). nutrient concentrations and high light penetration. Water column

Lyngbya, like other diazotrophs such as Trichodesmium, seems to stability and the natural buoyancy of Trichodesmium colonies (due

be particularly sensitive to the availability of iron (Fe), a to strong gas vesicles) aid in the development of vast, conspicuous,

component of the nitrogenase enzyme responsible for nitrogen surface blooms (Paerl, 1988; Capone et al., 1997). Blooms hundreds

ﬁxation (Kustka et al., 2003). It has been suggested that blooms of L. of kilometers in length have been observed in the Paciﬁc (Kuchler

majuscula in Moreton Bay may be due in part to anthropogenic and Jupp, 1988), Arabian Sea and Indian Ocean as well as the

disturbance via industry and land development of Fe rich acid- Caribbean and Gulf of Mexico (Capone et al., 1997). Such massive

sulphate soils, causing increased mobilization of iron from the aggregations of biomass have signiﬁcant impacts on nutrient

terrestrial to aquatic environments (Pointon et al., 2008; Albert cycling and ecosystem trophodynamics (Furnas et al., 1993; Karl

et al., 2005; Ahern et al., 2006b, 2007, 2008). Recently it has been et al., 2002). Trichodesmium has relatively slow growth rates

demonstrated that L. majuscula can use superoxide radicals to (doubling times of 3–5 days) which may be an adaptation for

obtain bio-available Fe by reducing Fe bound to organic ligands exploiting the high energy, but low nutrient conditions of the

(Rose et al., 2005; Rose and Waite, 2006), which may partially oligotrophic open oceans where blooms tend to form (Capone

explain its persistence in organic-rich waters such the Deception et al., 1997; Stal and Zehr, 2008). Trichodesmium is generally

Bay region of Moreton Bay (Albert et al., 2005; Ahern et al., 2007). outcompeted when it washes into coastal environments, but can

Addition of P, Fe and N have also been shown to increase thrive for periods of days to weeks causing large coastal blooms in

productivity, N2-ﬁxation and some secondary metabolites in L. tropical regions. When these blooms decay in enclosed coastal

majsucula in bioassays (Elmetri and Bell, 2004) as well as in ﬁeld environments, they can leach nutrients, organic matter, and water

studies in Guam (Kuffner and Paul, 2001) and Florida (Paerl et al., soluble toxins, consequently causing localized anoxia, ﬁsh kills and

2008), showing a consistency in factors affecting this species over mortality in marine organisms, including aquaculture species

broad geographic ranges. (Negri et al., 2004).

324 J.M. O’Neil et al. / Harmful Algae 14 (2012) 313–334

Trichodesmium has been widely studied due to its important blooms (Lenes et al., 2001; Pointon et al., 2008). There is some

role in biogeochemical cycling (Capone et al., 1997). The toxic indication that organic N derived from large Fe-driven Trichodes-

nature of Trichodesmium blooms, on the other hand, has received mium blooms can then in turn provide a N source from N2-ﬁxation

considerably less attention (Kerbrat et al., 2010, 2011) despite for other phytoplankton in the region including the red-tide

anecdotal evidence of its deleterious effects, including dermatitis dinoﬂagellate HAB species Karenia brevis in the Gulf of Mexico

in Belize called ‘‘pica pica’’ (Villareal, 1995) and asthma-like (Lenes et al., 2001; Walsh and Steidinger, 2001; Mulholland et al.,

symptoms in Brazil, called ‘‘Tamarande Fever’’ (Sato et al., 1963; 2006; Lenes and Heil, 2010).

Volterra and Conti, 2000). Similarly, beaches along the length of

Queensland, Australia are often closed due to Trichodesmium 5.2.2. Potential climate change effects

blooms that cause skin irritations, asthma-like symptoms and Trichodesmium is a tropical species that grows above 20 8C and

headaches (Stewart et al., 2007). A neurotoxic factor from thus may expand its range in the face of globally increasing

Trichodesmium was ﬁrst investigated by Hawser et al. (1991) in temperatures (Hutchins et al., 2007; Stal and Zehr, 2008). Recently

the Caribbean which was found to negatively impact zooplankton large blooms of Trichodesmium occurred in the vicinity of the

and prawn communities (Hawser et al., 1992; Guo and Tester, Canary Islands when sea-surface temperature exceeding 27.5 8C

1994; Preston et al., 1988). Further, ciguatera-like toxic effects promoted increased stratiﬁcation. Blooms had not previously been

were noted (Hahn and Capra, 1992), and compounds extracted recorded within this northwest African upwelling system (Ramos

from mackerel implicated in ciguatera-like poisonings in Queens- et al., 2005; Paul, 2008). Breitbarth et al. (2007) demonstrated that

land, Australia. These compounds were indistinguishable from the correlation of Trichodesmium blooms with temperature were

those found in T. erythraeum (Endean et al., 1993) with similar due to temperature-enhanced diazotrophic growth and suggested

ﬁndings more recently in New Caledonia (Kerbrat et al., 2010). In that the range and timing of Trichodesmium blooms may expand in

the last decade, MCY-LR (Ramos et al., 2005) and a MCY-like cyclic the future. Higher temperatures will also increase stratiﬁcation,

peptide (Shaw et al., 2004) have also been isolated from T. shoal the mixed layer, and suppress the upwelling of nitrate

erythraeum. More recently, analogs of MCY, cylindrospermopsin, (Doney, 2006), further promoting the growth of diazotrophic

and saxitoxin produced by Trichodesmium have been reported off organisms such as Trichodesmium.

the coast of Brazil (Proenc¸a et al., 2009), which will require lab There have been several recent studies demonstrating that

studies to conﬁrm. Trichodesmium experiences increased productivity, N2-ﬁxation

Researchers in New Caledonia following up on the earlier and/or growth under higher pCO2 levels (Barcelos e Ramos et al.,

‘‘ciguatera-like’’ toxin ﬁndings, made the breakthrough isolation 2007; Hutchins et al., 2007; Levitan et al., 2007, 2010a, 2010b,

and identiﬁcation of palytoxin and its derivative 42-hydroxy- 2010c; Kranz et al., 2010a, 2009, 2011). Trichodesmium may be

palytoxin (PLTXs) from both T. erythraeum and T. thiebautii. These chronically C limited under bloom conditions, when high rates of

compounds were not previously known to be produced by photosynthesis increase pH, as well as physical boundary layer

cyanobacteria, and had originally been isolated from the marine limitation (Kranz et al., 2010b). Therefore, under high light

zooxanthid Palythoa and the marine dinoﬂagellate Ostreopsis intensities and high CO2 levels, Trichodesmium shifts more energy

(Kerbrat et al., 2011). This is a significant finding, in that human to nitrogen fixation, rather than towards acquiring carbon

intoxications such as clupeotoxism (which has symptoms that (Hutchins et al., 2007). Collectively, ﬁndings regarding both

include: digestive disorders, paralysis, tachycardia, convulsions temperature and CO2 and Trichodesmium suggest this cyanobacte-

and respiratory distress) which occurs from eating plantivorous rium may be one of the ‘‘winners’’ in projected climate change

ﬁsh, could be cyanobacterial in origin, rather than previously being scenarios (Hutchins et al., 2007, 2009).

solely associated with Ostreopsis (Kerbrat et al., 2011). Researchers

have also found other benthic cyanobacteria responsible for local 5.3. Synechococcus

intoxication from the same lagoonal regions in New Caledonia

including Hormothonium lyngbyaceous, Oscillatoria, and Phormi- While Synechococcus is a cosmopolitan open ocean cyanobac-

dium (Laurent et al., 2008). More information is needed to better terium (Zwirglmaier et al., 2008), it also forms harmful blooms in

understand effects of cyanobacterial toxins on ecosystem tropho- multiple ecosystems including Florida Bay, USA (Walters et al.,

dynamics and human health. 1992; Boesch et al., 1993; Fourqurean and Robblee, 1999; Sunda

et al., 2006). These blooms cover large areas (100’s of square km)

5.2.1. Nutrients and can last for months. Negative ecosystem impacts include

Trichodesmium as a N2 ﬁxer, thrives in low nutrient environ- anoxic events and increased light attenuation (Phlips and Badylak,

ments, and is often limited by Fe or P (San˜udo-Wilhelmy et al., 1996; Phlips et al., 1999), which has reduced the distribution of

2001; Karl et al., 2002; Mills et al., 2004; Bell et al., 2005). Colonies seagrass beds and corals communities (Hall et al., 1999). The

can assimilate multiple species of N, including organic forms such blooms are also detrimental to ﬁsh (Boesch et al., 1993; Chasar

as urea and amino acids (Glibert and Bronk, 1994; Mulholland and et al., 2005), sponges (Butler et al., 1994; Peterson et al., 2006; Wall

Capone, 2001). Trichodesmium is capable of exploiting a variety of P et al., 2011), and spiny lobsters (Butler et al., 1995). Synechococcus

sources including inorganic phosphate, phosphomonoesters, and blooms are also known to inhibit zooplankton grazing (Goleski

phosphonate compounds (Dyhrman et al., 2006). Given its et al., 2010) due to the production of extracellular polysaccharides

diazotrophic nature, and adaptations for growth on a range of P and/or cellular toxins such as MCY (Mitsui et al., 1989; Phlips et al.,

sources at low levels, eutrophication in terms of N and P would not 1999; Carmichael and Li, 2006). The discovery of a haline strain of

be expected to promote Trichodesmium blooms. Iron, however, has microcystin-producing Synechococcus is signiﬁcant as production

been speculated to be able to increase Trichodesmium blooms on of this toxin has previously only been described in freshwater

large basin scales when large dust storms, from the Sahara deposit strains (Carmichael and Li, 2006).

Fe-rich particles as far as the Caribbean (Prospero, 1999, 2006;

Lenes et al., 2001; Prospero and Lamb, 2003). Therefore, conditions 5.3.1. Nutrients

such as ‘‘desertiﬁcation’’ (Takeda and Tsuda, 2005) due to climate Originally, nutrient loading had been hypothesized as a prime

change, drought or anthropogenic inﬂuences such as land clearing, cause of Synechococcus blooms in Florida Bay (Phlips et al., 1999)

that increase transport and deposition of Fe-rich aeolian dust may and has been the focus of water quality management and

result in increases in Trichodesmium and other cyanobacteria restoration efforts there (Boesch et al., 1993). However, reigning

J.M. O’Neil et al. / Harmful Algae 14 (2012) 313–334 325

algal paradigms support the concept that increased levels of 6. Synthesis and future directions

nutrients generally relieve the nutrient stress, and favor the

growth of larger phytoplankton (Raven and Kubler, 2002), As this review has demonstrated, cyanobacterial blooms are

suggesting that other factors could be contributing to the blooms promoted by higher temperatures and are often associated with

of small (1 mm) Synechococcus cells, including low predation high levels of anthropogenic nutrient loads, particularly with

rates. Consistent with this hypothesis, experimental inorganic regard to P. Paradoxically, however, most cyanobacteria are

nutrient loading to bloom waters in Florida Bay signiﬁcantly superior competitors for low levels of inorganic P and have highly

decreased the relative abundance of Synechococcus in the plankton reﬁned strategies for accessing P from organic compounds. These

(Goleski et al., 2010), suggesting that nutrient loading is likely to seemingly contradictory observations suggest that blooms of

discourage these blooms. Synechococcus blooms in Florida Bay are cyanobacteria occur as a sequence of events in temperate

known to exploit organic matter for growth (Glibert et al., 2004; ecosystems whereby blooms of other, non-cyanobacteria phyto-

Boyer et al., 2006) and are therefore more likely to dominate under plankton are likely to precede cyanobacterial blooms and

low inorganic nutrient conditions. These conclusions are also drawdown orthophosphate concentrations to low levels, a

consistent with the notion that the primary niche of picocyano- condition under which most cyanobacteria seem to thrive. As

bacteria is oligotrophic, open ocean environments (Agawin et al., the non-cyanobacteria phytoplankton are succeeded, die and/or

2000). are grazed, their biomass will be remineralized into organic forms

which most cyanobacteria are well adapted to exploit. In tropical

5.3.2. Potential climate change effects ecosystems, high temperatures promote the rapid microbial

Regarding climate change, Synechococcus achieves maximal assimilation of orthophosphate even in the face of high P loads,

growth rates at higher temperatures (30 8C) than other keeping concentrations chronically low, and favoring blooms of

cyanobacteria (Moore et al., 1995) and thus will potentially be cyanobacteria. Concurrently low levels of N will further favor

promoted by future climatic warming. This is consistent with the cyanobacteria that are diazotrophic and/or generally display

strong temperature dependence of Synechococcus in coastal highly ﬂexible N acquisition strategies. Since cyanobacterial

environments (Waterbury et al., 1986; Agawin et al., 1998; Gobler blooms typically occur under low CO2 conditions, future increases

et al., 2002). Synechococcus dominance may potentially be further in CO2 associated with climate change may suppress harmfual

promoted by warming-enhanced stratiﬁcation that minimizes cyanobacterial blooms, although research on this topic is in its

inorganic nutrient ﬂuxes to the upper mixed layer and maximizes infancy.

the importance of use of organic nutrient compounds. High The response of cyanobacteria to both eutrophication and

temperatures are likely to co-occur with high CO2 in the future. In global climate change effects (Fig. 2) are topics that will require

laboratory studies, Fu et al. (2007) found that increasing intense research focus in the future (Paul, 2008; Hudnell and

temperatures from 20 8C to 24 8C increased Synechococcus growth Dortch, 2008; Hudnell, 2008). Given the potential increase in the

rates and when combined with increasing CO2 concentration (from frequency and toxicity of cyanobacterial blooms in response to

380 ppm to 750 ppm) growth rates were further enhanced. Further both direct and indirect effects of changing climatic conditions

study is needed to fully clarify how future climate change may (Fig. 2), water management agencies will have to incorporate the

inﬂuence harmful blooms caused by Synechococcus. changing physical and chemical conditions of watersheds into

Fig. 2. Eutrophication and potenital effects of climate change on Cyanobacterial Harmful Algal bloom (CHAB) abundance.

326 J.M. O’Neil et al. / Harmful Algae 14 (2012) 313–334

remediation/management strategies which, to date, have primarily Cynthia Heil (FWRI/Bigelow Lab), Glen McGregor (GU), Hans

focused on nutrient reduction. As discussed in this review, increased Paerl (UNC-CH) and Christina Esplund-Lindquist (Kalmar Algae

warming of surface waters will impact the viscosity and stratiﬁca- Collection, Linnaeus University, Kalmar) kindly provided photo-

tion of water columns. This will have a direct impact on the duration micrographs. Support was received from the following sources:

of hypoxic conditions in bottom waters of systems (i.e. Baltic Sea; JO’N and CJG’s efforts were supported by the NOAA-ECOHAB

Lake Erie, USA), nutrient cycling within the hypoxic zones (i.e. P, Fe) program funded by the National Oceanic and Atmospheric

as well as have a signiﬁcant impact on competition within the Administration Center for Sponsored Coastal Ocean Research

plankton community in surface waters and, therefore, must be (JO’N subaward #NA06NOS4780246 to UMCES; CJG under award

considered in future management plans. Furthermore, changing #NA10NOS4780140 to Stony Brook University); TWD and MAB’s

climatic conditions will potentially alter rainfall patterns and thus efforts were supported by an Australian Research Council

the delivery of nutrients into aquatic ecosystems. Two scenarios are Linkage grant and the Australian Rivers Institute. We would

possible in different regions: (1) storms and rainfall will increase, like to thank Drs. William Dennison, Matthew J. Harke, Linda

lead to enhanced freshwater delivery of nutrients and decreased Tonk and Susie Wood for constructive comments on the

residence time, which may or may not stimulate harmful manuscript. JO’N thanks Hoegh-Guldberg and the University of

cyanobacterial blooms or other HAB species, depending on the Queensland Global Change Institute for use of facilities and

physical factors including light and temperature; or (2) While such library while writing this review. This is UMCES Contribution #

increased ﬂow could initially suppress blooms by decreased 4565.[SS]

residence times, increased turbidity and a reduction in stratiﬁcation,

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